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Home , Citrus canker, Kinnow, Xanthomonas, Xanthomonas campestris

J. Appl. Hort.,5(1):52-60, January-June, 2003

Citrus canker – A review

A.K. Das National Research Centre for , Amravati Road, PO Box 464, Nagpur-440 010, Maharashtra, .

Abstract Of all the agricultural pests and diseases that threaten citrus crops, is one of the most devastating. The disease, caused by the bacterium axonopodis pv. citri, occurs in large areas of the world's citrus growing countries including India. At least 3 distinct forms or types of citrus canker are recognized. Among these, Asiatic form (Canker A) is the most destructive and affects most of the major citrus . Severe infection of the disease produces a variety of effects including defoliation, dieback, severely blemished , reduced fruit quality and premature fruit drop. Warm, humid, cloudy climate, along with heavy rainfall and strong wind promotes the disease. Control of canker in countries or regions where the disease is not present include quarantine or regulatory programme to prohibit introduction of infected citrus material and fruit, as well as continuous and strict surveying in the field and the immediate destruction of infected trees. In countries where canker is present, integrated systems of compatible cultural practices and phytosanitary measures consisting of resistant hosts, removal of inoculum sources, properly designed windbreak systems, timely application of protective copper-containing and/or antibiotic sprays are generally the most effective means of disease management. This paper reviews the current state of knowledge and understanding on pathogens and strains associated with the disease and their identification, host-pathogen interaction, molecular mechanism of pathogenicity, epidemiological aspects and management practices.

Key words : Citrus canker, Xanthomonas axonopodis pv. citri, pathogen, strain, epidemiology, disease management

Citrus canker is one of the most feared of citrus diseases, affecting States region of USA in 1915. The Gulf States outbreak is believed all types of important citrus crops. The disease causes extensive to have resulted from a shipment of infected nursery stock from damage to citrus and severity of this infection varies with different Asia (Dopson, 1964). The disease also appeared earlier this century and varieties and the prevailing climatic conditions. The in South America (Rossetti, 1977), South Africa (Doidge, 1916) disease is endemic in India, and other South- East Asian and Australia (Garnsey et al, 1979). The disease was reportedly countries, from where it has spread to all other citrus producing eliminated in these countries as well as the Gulf States through continents except Europe. Generally canker does not occur in nursery and orchard inspections, quarantines, and the on-site arid citrus growing areas and has been eradicated from some burning of infected trees. Subsequent epidemics have occurred in areas. However, widespread occurrence of the disease in many Argentina, Australia, , , , Reunion Island, areas is a continuous threat to citriculture especially in canker- the USA, and Uruguay. In some locations, eradication efforts have free areas. Intensive research on citrus canker is being carried been attempted and failed. In others, active eradication campaigns out throughout the world which has been reviewed by Rossetti continue (, Uruguay, Brazil) (Schubert and Miller, 2000). (1977), Civerolo (1981,1984), Chand and Pal (1982), Schoulties et In India, citrus occupies third position among after mango al. (1987), Stall and Civerolo (1991) and Goto (1992). However, all and and canker is one of the major constraints of its these reviews are either brief, restricted to one country, or by now out of date. This review aims to present an overview of cultivation. Citrus canker was first reported from (Luthra citrus canker worldwide with special reference to India. and Sattar, 1942; Bedi, 1961). Its occurrence was further recorded in Tamil Nadu (Ramakrishnan, 1954) , Andhra Pradesh (Govinda Origin and history: The geographical origin of citrus canker is a Rao,1954), Karnataka (Venkatakrishnaiah,1957; Aiyappa,1958), matter of controversy. Lee (1918) reported that it may have arisen Rajasthan (Prasad,1959), Madhya Pradesh (Parsai,1959), Assam in southern China, and he assumed Fortunella hindsii to be the (Chowdhury,1951) and Uttar Pradesh (Nirvan, 1960). Several others wild host plant. However, Fawcett and Jenkins (1933) reported have reported the incidence of canker on the acid and other that citrus canker originated in India and Java, rather than in varieties of citrus. Further, the disease appear as a serious problem other regions of the Orient, because they detected canker lesions whereever acid lime (C. aurantifolia) is grown on a large and on the oldest citrus herbaria kept at the Herbaria of the Royal commercial scale (e.g., Akola region in central India, Nellore and Botanic Gardens in Kew, England (i.e., Citrus medica collected Periyakulum regions in southern India and Khera region of western from India in 1827-1831 and C.aurantifolia from in India) and has become a permanent major problem to the citrus 1842-1844). These findings suggest the origin of disease in the growers of this country. Recently canker has been detected in tropical areas of Asia, such as South China, Indonesia, and India, mandarin nursery in the state of Punjab (Anonymous, 2000). where Citrus species are presumed to have originated and to have been distributed to other citrus- growing areas in the form Distribution and economic importance: In spite of the heightened of budwood. Citrus canker was described afterwards in the Gulf regulations imposed by many countries to prevent introduction, Citrus canker – A review 53

In spite of this effort, the disease continues to spread in the Miami area of Florida,USA (Schubert and Miller, 2000) and hence some researchers, growers and residents are disputing the concept and feasibility of eradication. Forms: There are three different forms of citrus canker disease caused by various pathovars and variants of the bacterium Xanthomonas axonopodis Starr and Garces emend. Vauterin et al.(1995). Differentiation of these forms is mainly based on geographical distribution and host range of the pathogen (Stall and Seymour, 1983). The Asiatic form of canker (canker Fig. 1. Distribution map of citrus canker (Xanthomonas axonopodis pv. citri) A, cancrosis A or true canker), caused by X. axonopodis pv. citri (Hasse) Vauterin (Xac) is the most common, widespread the disease continues to increase its geographic range. Citrus and severe form of the disease. The disease is endemic throughout canker presently occurs in over thirty countries in Asia, the Pacific India, , the islands of Indian Ocean, South-East Asia, and Indian Ocean islands, South America, and the Southeastern China and Japan. Cancrosis B (canker B or false canker), caused USA (Fig. 1). by X. axonopodis pv. aurantifolii (Hasse) Gabriel Vauterin is a The economic importance of citrus canker can be analyzed from serious problem on in Argentina, Paraguay and Uraguay. several different points of view. Loss assessment has not been Mexican lime, sour , and pummelo are also susceptible. determined clearly, as in the case of diseases of annual crops. Cancrosis B causes canker-type lesions on fruit, leaves, and twigs When citrus infection occurs in the early growing stage, the that are similar to but smaller than those produced by the A form. fruits crack or become malformed as they grow, and the heavily In culture, cancrosis B grow more slowly than canker A infected ones fall prematurely. Light infection in later growth bacteria on nutrient agar, and a specific medium containing stages may cause only scattered canker lesions on the surface of sucrose, peptone, salts, and purified agar has been developed fruits but makes fresh fruits unacceptable for market. The severity for this form. Cancrosis B isolates can be differentiated of fruit infection usually parallels that of foliage infection. Eighty serologically from the canker A bacteria but not from Cancrosis to ninety percent of fruit infection is not uncommon in susceptible C isolates. Cancrosis C, also caused by X. axonopodis pv. citrus trees that have already sustained severe foliage infection. aurantifolii, has been isolated from Mexican lime in Brazil. Such heavy foliage infection often causes severe defoliation, Symptoms are the same as those of canker A. In 1984, a new leaving only bare twigs (Goto,1992). In Argentina, for example, xanthomonad disease of citrus was discovered in Florida nurseries. 83-97% of the fruit of trees were diseased in unsprayed The causal bacterium is shown to have no relationship to the plots during 1979-1980 and in the same plots, upto 88% of the existing two pathovars of Xanthomonas axonopodis (causing leaves were infected (Stall and Seymour, 1983). canker A, B and C) and named as Xanthomonas axonopodis pv. (Hasse) Gabriel Vauterin (earlier called group E canker or Worldwide, millions of dollars are spent annually on prevention, canker E). The disease is most commonly referred to as citrus quarantines, eradication programs, and disease control. bacterial spot (CBS). At present CBS is only known from Florida, Undoubtedly, the most serious consequence of citrus canker where it appears to be restricted entirely to nurseries (Gottwald infestation is the impact on commerce resulting from restrictions and Graham, 2000). The differential characteristics of the three to interstate and international transport and sale of fruit originating forms of citrus canker and CBS are given in Table 1. from infested areas. The disease has been studied in greater detail in the U.S. where it caused very serious damage, so much Other forms of citrus canker have also been reported. For example, so that millions of canker affected trees were cut and burnt. In canker D, sometimes called citrus bacteriosis, was reported in the Florida, for example, during the year 1915-33, nearly 2,57,000 Colima area of Mexico in 1980s (Rodriquez et al.,1985) but later it orchard trees and 3,000,000 nursery were destroyed at a was found to be caused by Alternaria limicola. An isolate of cost of over $ 6 million and again during the year 1984-86, nearly Xanthomonas was discovered in Oman in 1986 that produced 20 million citrus nursery plants were destroyed at a cost of over canker A-like lesions only on Mexican lime. Similar isolates $ 25 million (Schoulties et al., 1987). Presently over $ 12 million (known as A*) have been found in Saudi Arabia, , and India per year and over 600 personnel are dedicated to this programme. (Verniere et al.,1998). Another atypical form of canker A bacteria,

Table 1. Comparison of three different forms of citrus canker and citrus bacterial spot (CBS) of citrus Characteristics Citrus Canker Citrus bacterial spot (CBS) Canker form A B C Pathogen X. axonopodis pv. citri X. axonopodis pv. aurantifolii X. axonopodis pv.aurantifolii X. axonopodis pv. citrumelo Distribution Asia, Africa,South Argentina, Paraguay, Uruguay Brazil, Mexico America (Florida) AmericaOceania Host range Wide Limited Limited Wide Major host plant Citrus spp. Mexican lime Citrus spp. (nursery) Symptoms Spongy erupted at first; corky rough lesions with a raised, greasy margin Flat or sunken lesion; extreme later; water-soaked appearance water soaking Modified from Goto (1992) 54 Citrus canker – A review

which has high levels of resistance to penicillin related antibiotics, periods of heavy rainfall, high temperatures and growth flushes. has been described from Reunion and surrounding islands in the Host range and varietal susceptibility: Civerolo (1984) lists a Indian Ocean (Gottwald and Graham, 2000). number of plants in the family rutaceae other than Citrus and Symptoms: The diseased plants are characterized by the Poncirus that can serve as hosts of Xac under experimental occurrence of conspicuous raised necrotic lesions that develop conditions or heavy disease pressure in nature. Among on leaves, twigs and fruits. Lesions can be detected by drawing commercial citrus varieties and rootstocks, Asiatic citrus canker the fingers over the surface of infected tissues. On leaves, first is most severe on grapefruit (C. paradisi), limes (C. aurantifolia, appearance is as oily looking, 2-10 mm circular spots, usually on C. limettioides), (Poncirus trifoliata) and their the abaxial surface (reflecting stomatal entry following rain hybrids because of their high susceptibility (Table 2). dispersal). Lesions are often similarly sized. Later, both epidermal In India, citrus canker is reported to be relatively more on acid surfaces may become ruptured by tissue hyperplasia induced by lime and less commonly on mandarin and sweet orange the pathogen. On leaves, stems, thorns and fruit, circular lesions (Ramakrishnan, 1954). According to Aiyappa (1958) all the become raised and blister-like, growing into white or yellow cultivated varieties of citrus and some wild species in Karnataka spongy pustules. These pustules then darken and thicken into a are suspectible to canker possibly due to heavy rainfall, high light tan to brown corky canker, which is rough to the touch. humidity and low temperature. Prasad (1959) from Rajasthan made Often a water- soaked margin develops around the necrotic tissue similar observations. The descending order of susceptibility in and is easily viewed with transmitted light. On stems, pustules citrus species is Kaghzi Lime, grape fruit, Karnakhata and sweet may coalesce to split the epidermis along the stem length, and oranges (Nirvan, 1961). Mandarins and lemons are resistant and occasionally girdling of young stems may occur. Older lesions are commercially immune under conditions existing in on leaves and fruit tend to have more elevated margins and are at Uttar Pradesh. Jain (1959) reported that different varieties of sweet times surrounded by a yellow chlorotic halo (that may disappear lime, grape fruit and sweet orange were infected almost to same as canker lesions age) and a sunken center. Sunken centers are extent in Himachal Pradesh. According to Naik (1949) acid limes, especially noticeable on fruits, but the lesions do not penetrate some varieties of lemon, sweet orange and grapefruit were very far into the rind thereby not affecting internal quality. Severe susceptible to canker, while Nepali oblong and round seedless infection results in defoliation, die-back, deformation of fruit and lemons were highly resistant. Mundkur (1961) observed no infection premature fruit drop (Rossetti, 1977; Civerolo, 1981; Chand and in sweet orange and pummelo but Jambheri, sour orange and Kaghzi Pal, 1982; Stall and Seymour, 1983). Canker causes fruit losses lime were very susceptible. ranging from premature fruit drop due to abscission to non marketable quality due to lesions. Disease of the fruit is probably Host- pathogen interaction: Citrus canker research has been the most economically important damage since fruits with canker primarily oriented toward the ecological behaviour of the causal lesion are not acceptable for fresh market and fetch very little bacterium. Studies from physiological and biochemical standpoint price. are therefore very limited. An essential diagnostic symptom of the disease is citrus tissue Xac produces abundant extracellular polysaccharides (EPS), both hyperplasia (excessive mitotic cell divisions), resulting in cankers in culture media and in host tissues. The bacterial cells in canker (Gabriel et al., 2000). Canker symptoms on leaves and fruit can be lesions are embedded in a dense matrix of EPS and are dispersed, readily obtained by artificial inoculations. If cankers are not together with EPS, by rain splash. The EPS molecules exhibit present on leaves, stems and fruit of mature trees, or if leaves and great protective effects against the 'dilution effect' in water and fruit of susceptible Citrus species do not develop cankers desiccation in air, providing benefits for the bacterial ecology following artificial inoculation, a diagnosis of citrus canker is not (Goto, 1985). After entering the intercellular space (through indicated. Occurrence of lesions is seasonal, coinciding with stomata or wounds) they adhere to the host cell walls through an interaction between bacterial EPS and citrus agglutinins Table 2. Susceptibility of several citrus varieties and rootstocks to Xanthomonas (Takahashi and Doke, 1984). Ethylene production by axonopodis pv. citri citrus leaves inoculated with Xac and increased concentration of indole acetic acid (IAA) in the Xac Highly Susceptible Moderately Susceptible inoculated leaves have also been reported (Goto et Citrus paradisi Macf., grapefruit C. sinensis (L.) Osbeck, sweet orange al., 1979a). C. aurantifolia (Christ.) Swingle, acid lime C. aurantium L., sour orange C. limettioides Tan., Palestine sweet lime C. limon (L.) Burm., lemon Padmanabhan et al. (1973) studied the physiology Poncirus trifoliata (L.) Raf., trifoliate orange C. J. Ingram & H.E. Moore, of canker infected citrus leaves with special reference tangelo to halo formation, and reported that halo zone Moderately Resistant Highly Resistant respired more than the cankered tissue. Catalase C. reticulata Blanco, mandarin, C. medica L., activity was very high in the halo region. Both C. maxima (Burm.) Merr., pummelo microcarpa (Bunge) peroxidase and ascorbic acid-oxidase activity Wijnands, calamondin increased in canker as well as in halo regions. They C. aurantifolia (Christ.) Swingle, Person Fortunella spp., again recorded a descrease in chlorophyll a, b, carotene and xanthophyll contents in the canker, halo or Tahiti lime and pre-halo regions of the citrus leaves infected by Recently, it was reported that goat weed (Ageratum conyzoides L.) could serve as a host canker-inducing bacterium. Photosynthesis was of Xac. This plant is common in citrus orchards in the state of Assam in India (Kalita et al. impaired in the infected regions while starch content 1997). This represents the only report of a non-Rutaceous host of Xac. was not affected in the halo regions (Padmanabhan Citrus canker – A review 55

et al., 1974). Total sugar content decreased in all the infected also observed strain variation in Xac. Recently Das (2002) reported regions. Kishore and Chand (1972, 1975) carried out biochemical the existence of pathogenic variability within the 'A' strain of analysis of healthy and canker infected leaves and reported that Xac. amino acid content decreased in infected leaves. They also noticed Pathogen and strain identification: Because symptoms are more total phenols in resistant C. reticulata than in susceptible generally similar, identification and separation of canker C. aurantifolia. pathogens and strains are based on cultural and physiological Pathogen biology characteristics (Schaad,1988), bacteriophage sensitivity (Goto et al., 1980; Civerolo, 1984), serology (Alvarez et al., 1991), plasmid Pathogens and strains: Based on currently available information, fingerprints (Pruvost et al., 1992), DNA- DNA homology (Egel et at least three pathovars (sometimes called strains) of al.,1991) and by various RFLP (restriction fragment length Xanthomonas axonopodis have been recognized. These polymorphism) and PCR (polymerase chain reaction) analyses pathovars are distinguished from one another by geographical (Gabriel et al., 1988; Hartung and Civerolo, 1989; Gillings et al., distribution and by different pathogenicity to members of genus 1995; Hartung et al., 1996; Miyoshi et al., 1998; Cubero and Citrus.The pathogen for canker A was first identified and Graham, 2002). When the DNA-based assays are unavailable, described as citri by Hasse (1915). Bacterial strains of Xac can be distinguished from other pathovars by nomenclature has undergone many changes since then and the infecting a panel of susceptible and resistant citrus hosts or as a causal bacterium is now known as Xanthomonas axonopodis bioassay on detached-leaves or leaf-disks (Gottwald et al., 1993). pv. citri (Hasse) Vauterin [Syns. X. citri (Hasse) Dowson and X. Such pathogenecity test is an essential component in diagnostic campestris pv. citri (Hasse) Dye] (Dye et al., 1980; Vauterin et programmes for regulation of citrus canker diseases (Schubert et al.,1995). The pathogen for canker B and C and other related al., 2001). strains associated with the disease have already been discussed (see Forms). Pathogenecity: Identical symptoms induced by two taxonomically distinct groups of strains (canker A and B) are The bacterium (Xac) is rod-shaped measuring 1.5-2.0 x 0.5-0.75 indicative of a common pathogenicity factor. Gene pthA is µm, Gram-negative, and has a single polar flagellum. Growth is essential for Xac to elicit cankers on citrus, and pthA confers this obligately aerobic. Colonies on culture media are usually yellow ability to various X. axonopodis strains (for example, pathovars as a result of xanthomonadin pigment production. When glucose alfalfae and citrumelo) ( Swarup et al.,1991; Swarup et al.,1992). or other sugars are added to the culture medium, colonies become Functionally homologous genes (pthB and pthC) have also been very mucoid due to the production of an extracellular identified and cloned from X. axonopodis pv. aurantifolii polysaccaride slime. The optimum temperature range for growth pathotype B and pathotype C, respectively (Gabriel et al., 2000). is 28 to 30° C (82 to 860 F), and the maximum temperature range for Both pthB and pthC are essential for X. axonopodis pv. aurantifolii growth is 35 to 390 C (95 to 1020 F). Bacterial cells are positive for pathotypes B and C, respectively, to cause cankers on citrus, hydrolysis of starch, aesculin, casein, liquefaction of gelatin, and pthB and pthC confer this ability to various X. axonopodis and production of tyrosinase, catalase, reducing substance from strains. All three genes are therefore functionally interchangeable, sucrose, and hydrogen sulfide. The bacterium is negative for and these genes may have been transferred horizontally on nitrate reduction, indole production and for methyl red test (Chand plasmids between Xac and X. axonopodis pv. aurantifolii strains. and Pal, 1982; Goto, 1992). Genes pthA, pthB and pthC are all members of an avirulence / Goto (1969) in Japan, differentiated 300 isolates of X. citri into 5 pathogenicity gene family widely distributed in the genus strains by their ability to oxidise mannitol and lactose, and by Xanthomonas (Swarup et al.,1992; De Feyter et al.,1993). Genes rapidity of breakdown of mannose. In Argentina, two biotypes pthA, pthB and pthC, when transferred into Xac, X. axonopodis were distinguished among 65 isolates of Xac based on growth pv. aurantifolii or X. axonopodis pv. citrumelo, confer ability to on media with carbohydrates, acid production in litmus milk and elicit hyperplasia (cell divisions or cankers) on all citrus species colony appearance in wakimoto’s medium (Falico de Alcaraz, in the normal host range of the recipient strain. Mutations of 1980). Goto et al. (1980) distingushed canker A strain from the B genes encoding either the protein injection system of the strain by bactoriophage sensitivity test. A strains are susceptible pathogen (a type III secretion system encoded by hrp genes) or to lysis by phage CP 1 or CP 2 while B strains are susceptible to the effector molecule, pth A/B/C, abolish pathogenicity of canker lysis by CP 3. Civerolo and Fan (1982) successfully employed bacteria (Gabriel et al., 2000). ELISA to identify the different strains of Xac. Alverez et al. (1991) Disease cycle and epidemiology produced monoclonal antibodies for A, B and C-form pathogens and noticed that canker A MAb did not react with strains Survival: Xac survives primarily in naturally occurring lesions. associated with other forms of citrus canker (B,C). Cankerous leaves, twigs and branches constitute the main source of inoculum. Since affected leaves drop early, they may not serve In India, occurrence of strains (pathotypes) of the pathogen has as the main source of inoculum (Nirvan, 1963), but Rao and been reported by Rangaswami and Soumini (1957) and Hamlin Hingorani (1963) found that the bacterium survives upto 6 months (1967). Khan and Hingorani (1970) grouped 15 isolates of the in the infected leaves. The disease is carried from season to pathogens into 3 strains by their reaction on Murraya exotica. season mainly in the cankers on twigs and branches. The Kishore and Chand (1972) studied the reaction of eight isolates pathogen can survive in diseased twigs upto 76 months on C. aurantifolia, C. sinensis and C. jambhiri and showed the (Chakravarti et al, 1966). Vasudeva (1958) found that the organism presence of more than one strain of the pathogens in Harayana. survived in the infected leaves for more than six months, in the Similarly Prasad et al. (1978) and Buragohain and Chand (1991) sterilized soils for 52 days and in the unsterilized soils for 9 days 56 Citrus canker – A review

only. Under desiccation at 30 0C, he found the organism surviving but there is no authenticated record of this having happened. for 11 or 12 days. Paracer (1961) observed that the bacterium was Nursery workers can carry bacteria from one nursery to another resistant to drying and was killed after 120 days in ordinary on hands, clothes, and equipment. Similarly, spread can also result laboratory temperature. from movement of contaminated budwood or contaminated budding equipment. Pruning, hedging, and spray equipment have The bacterium also survives epiphytically at lower population been demonstrated to spread the bacteria within and among levels on citrus hosts without symptom development, in plantings. Wooden harvesting boxes that contained diseased association with non-citrus weed and grass hosts and also in fruit and leaves have also been implicated in long-distance spread. soil (Goto, 1970, 1972, Leite and Mohan, 1984). But saprophytic survival of Xac in soil in absence of plant tissue or debris has Temperature between 200 to 300C with evenly distributed rains not been conclusively established (Goto, 1970). Graham (1989) are most suitable for the disease (Ramakrishnan,1954; Reddy, reported that population of Xac have very limited survival 1984). As Peltier and Frederich (1926) pointed out, citrus canker capability in subtropical soils. Attempts to detect surviving is severe in regions where temperature and rainfall ascend and bacteria on various inanimate surfaces such as metal, plastics, descend together during the year. Therefore the disease occurs cloth and processed wood in both shade and sun indicate the in severe form in seasons and/or areas characterized by warm inoculum dies within 24-72 hours (Graham et al., 2000). and humid weather conditions. Infection: Bacterial cells ooze from existing lesions during wet Leafminer interaction: The Asian leafminer, Phyllocnistis weather to provide inoculum for further disease development. citrella Stainton, can infest leaves, stems, and fruit and greatly Infection by Xac occurs, like many other bacterial diseases, increase the number of individual lesions which quickly coalesce primarily through stomatas, and wounds produced during strong and form large irregular shaped lesions that follow the outlines of winds and by insects. Resistance of leaves, stems and fruits the feeding galleries. Leafminers wound leaves when they begin generally increases with tissue maturation. The period of feeding. The feeding galleries are just below the epidermis. When susceptibility to wound infection may be longer than that for the galleries become contaminated with citrus canker bacteria, stomatal infection, depending on the (Goto, 1962). Lesion numerous infections can occur, resulting in tremendous inoculum development and bacterial multiplication may be directly related production and canker infection (Nirvan, 1961; Sohi and Sandhu, to host resistance (Koizumi, 1979). However, the number of Xac 1968; Sinha et al.,1972; Cook, 1988). Trees with wounds caused cells per lesion may not always be correlated with host plant by leaf miner remain susceptible for 7-14 days compared to only resistance (Stall et al., 1980). Presence of free moisture on the 24 hours for wounds caused by wind, thorns or pruning (Filho host surface for 20 min. is essential for successful infection and Hughes, 2000).However, there are no published data that the (Ramakrishnan, 1954). leafminer serves as a true vector of canker inoculum. Leaves, stems, and fruit become resistant to infection as they Disease management: Commercially acceptable management of mature. Almost all infections occur on leaves and stems within canker, especially on susceptible cultivars under favourable the first 6 weeks after initiation of growth. Leaves are most disease development conditions, is generally difficult. The most susceptible when expanded between 50 and 80% (Filho and effective management of canker is by supplementing the use of Hughes, 2000). The most critical period for fruit infection is during resistant cultivars with integrated systems of compatible cultural the first 90 days after petal fall. Any infection that occurs after practices and phytosanitary measures, including quarantine and this time results in the formation of only small and inconspicuous regulatory programmes. The basic strategies of the specific pustules. Because the fruit are susceptible over longer time methods are to avoid, exclude, or eradicate the pathogen, to reduce periods than leaves, infections can result from more than one the amount of inoculum available for infection, to minimize dispersal event. As a result, lesions of different ages can be dissemination of the pathogen, and to protect susceptible tissue found on the same fruit (Gottwald and Graham, 2000). from infection (Civerolo, 1981). In canker-free citrus producing areas, strict quarantine measures are practised aimed at excluding Dispersal: Since Xanthomonads have mucilaginous coat, they the pathogen. When the canker bacterium is introduced into easily suspend in water and are dispersed in droplets. Spread of such an areas (as it was in Florida, USA in 1910, 1984 and 1995) canker bacteria by wind and rain is mostly over short distances, eradication campaign is conducted by uprooting and burning all i.e., within trees or to neighbouring trees. Cankers develop more suspected and infected trees. A new regulation - the "1900-ft. severely on the side of the tree exposed to wind-driven rain. rule" is established recently in USA, requiring the removal and Rainwater collected from foliage with lesions contains bacterial destruction of diseased citrus trees and of all healthy citrus trees population between 105-108 cfu/ml (Goto, 1962; Stall et al., 1980). within a 1900-ft radius of a diseased tree (Gottwald et al., 2002). If the average wind speed during rains exceeds 8 m/sec (18 mph), the disease may be very severe (Kuhara, 1978). Wind blown But under endemic condition (like that which exists in India) inoculum was detected upto 32 meters from infected trees in such an eradication measure is considered not feasible. Here Argentina (Stall et al., 1982). Spread over longer distances, up to conditions are favourable for disease development during the 7 miles, can occur during severe tropical storms, hurricanes, and major part of the year. Hence effective control of this disease tornadoes (Gottwald et al., 2001). Long-distance spread more depends on the continuous care and attention paid by the grower. often occurs with the movement of diseased propagating material, Canker incidence under these conditions can be reduced such as budwood, rootstock seedlings, or budded trees. considerably by taking integrated management approach There is no record of seed transmission. Commercial shipments consisting of (i) using canker-free nursery stock, (ii) Pruning all of diseased fruit are potentially a means of long-distance spread, the infected twigs before monsoon and burning them, (iii) Citrus canker – A review 57

periodical spraying of suitable copper-based bactericides (to observed to reduce lesions numbers on fruit but not on leaves reduce inoculum build-up on new flushes and to protect (Timmer, 1988). Where copper resistance was found expanding fruit surfaces from infection) alongwith an insecticide recommendation include addition of mancozeb to the copper (to control insect injury), (iv) taking some precautions to reduce sprays (Canteros, 2000). When canker occurred in the USA, the the risk of spread of disease in orchards and nurseries and (v) by emphasis was on eradication, and other measures for control of evolving canker-resistant varieties suited to local environmental canker were not adequately researched (Stall and Civerolo,1991). conditions (Das and Singh,1999, 2001). However, recently in Florida, USA, some induced systemic Fawcett (1936), Naik (1949), Cheema et al. (1954), Ramakrishnan resistance (ISR) compounds (e.g. Messenger, Nutri-phite, Oxycom (1954), Govinda Rao (1954), Prasad (1959) and Paracer (1961) and FNX-100) are under evaluation for their potential to control recommended pruning of infected twigs before the onset of canker A using citrus bacterial spot on swingle citrumelo as a monsoon and spraying of 1% Bordeaux mixture at periodical surrogate pathosystem (Graham et al., 2000). intervals for an effective control of the disease. Patel and Desai In India, where canker disease has established since a long period (1970) reported that pruning of affected twigs every year during it was suggested that resistant varieties and species should be Nov-Dec and 3 to 4 sprays of Bordeaux mixture (1%) in a year grown (Mundkur, 1961). Here canker infestation is relatively more could reduce the disease. Two prunings alongwith 4 sprays of on acid lime and less common on mandarin and sweet orange. 5000 ppm copper oxychloride or 1% Bordeaux mixture is reported Kumquat (Fortunella spp.) and Hazara Narangi (C. microcarpa) to be effective against the disease (Kishun and Chand, 1987). are commonly grown in India for ornamental purpose and these Other chemicals found effective against the canker were perenox are found resistant to canker. C. latifolia was also found to be (Chowdhury,1951), Ultrasulphur (Nirvan, 1961), mixture of sodium resistant to the disease (Kishun and Chand, 1987). Although arsenate and copper sulphate (Patel and Padhya, 1964), Blitox several acid lime selection/clone or hybrids have been claimed and nickel chloride (Ram et al.,1972). According to Rangaswami either as resistant or tolerant from different regions e.g. RHR-L- et al. (1959), 500-1000 ppm streptomycin sulphate was effective 49 (Sai Sarbati) (Desai et al.,1999), Tenali (Madhavi et al., 2000), when sprayed with 1% glycerine on acid lime. Six sprays of 1000 ALH-77 (lime x lemon hybrid) (Prasad et al., 1997), these need to ppm streptomycin sulphate along with two prunings reduced the be tested through multilocational trials. canker in acid lime (Balaraman and Purushotman, 1981). Other effective antibiotics were Agrimycin (Sawant et al., 1985), Studies on biological control of citrus canker are still in a Streptocycline (Mathur et al., 1973) and Streptocycline in preliminary stage. Some strains of bacteria viz., Pseudomonas combination with Bordeaux mixture (Krishna and Nema, 1983). syringae, Erwinia herbicola, Bacillus subtilis and Pseudomonas Kale et al. (1988), in field trials with 7 different chemicals, found fluorescence isolated from citrus phylloplane were reported to that the best control of Xac was given by Paushamycin + Blitox be antagonistic in vitro to the canker pathogen (Ota, 1983; Goto followed by Bordeaux mixture. Application of neem cake solution et al., 1979b; Kalita et al., 1996; Unnimalai and Gnanamanickam, on the foliage reduced the canker in nurseries (Dakshinamurthi 1984). However, it seems difficult to find antagonistic bacteria and Rao, 1959; Reddy and Rao, 1960). Kale et al. (1994) suggested that reside stably on smooth surfaces of mature citrus leaves. that for better control of canker, spraying of streptocycline + Future prospects: Citrus canker continues to be the cause of Copper oxychloride (0.1%) should preferably be done at 7 days worldwide concern as a potentially hazardous threat to citriculture. or 15 days interval. Integrated application of pruning of infected There is a wide range of physiological, biochemical, serological, twigs, Copper oxychloride (0.3%), streptocycline (100ppm) and molecular and pathogenic variation among strains of bacteria neem cake suspension was found very effective in controlling associated with citrus canker. Moreover new strains are the disease (Das and Singh, 2000). Canker incidence can also be originating regularly as a result of mutation. A better reduced by periodic spraying of insecticides to control of leaf understanding of the pathogenic specialization and proper miner damage to newly unfolded leaves, as such damage facilitates identification of Xac strains are needed. This could be important citrus canker infection. also for breeding new canker resistant cultivars. The development Control measures developed in Japan include windbreaks of effective chemicals for control of citrus canker has been long (Koizumi et al., 1996) or pruning of diseased summer and autumn claimed by citrus growers and pathologists. However, these shoots, forecasting and chemical sprays. Six or seven sprays of efforts have actually been unsuccessful, as has been the case copper are necessary to protect new growth from infection with other plant bacterial diseases in general. Most chemicals (Kuhara, 1978). In China control measure consists of spraying with great effectiveness in vitro do not necessarily show copper ammonium WC during summer and autumn months satisfactory effects. The gaps found between effectiveness in (Chen,1998). Gottwald and Timmer (1995) reported the efficacy of vitro and in situ may stem in part from the mode of bacterial wind- breaks in reducing the spread of citrus canker in Argentina. infection. Under rainy conditions, some bacterial cells may McGuire (1988) evaluated 13 bactericidal chemicals over 3 seasons achieve direct access to the front cavity of stomata or to wounds on 3 citrus species to determine their ability to control canker. In without being exposed to the protective chemicals left on the leaf field trials conducted in Argentina, he noticed copper ammonium surface. Therefore, for development of effective bactericides, carbonate with 8% metallic copper was consistently superior to emphasis must be placed on the effectiveness of chemicals other products in controling Xac. In another field test on mature reaching at least to the depth of the stomatal cavity. Recent findings grapefruit trees, three applications per seasons of copper have demonstrated that the plants usually carry the internal ammonium carbonate (CAC) or copper hydroxide + maneb were resident microbes (endophyte) in vascular systems. There is a 58 Citrus canker – A review substantial possibility that an antagonistic microbe may be found Das, A.K. and Shyam Singh, 1999. Management of Bacterial Canker in among these endophytes which will be useful in biological control Acid lime. Intensive Agriculture, 36(11-12): 28-29. of citrus canker. Fresh approaches are also to be made to develop Das, A.K. and Shyam Singh, 2001. Managing citrus bacterial diseases in environmentally safe methods to combat this bacterium viz. search the state of Maharashtra. Indian Hort., 46(2): 11-13. for its resistance in wild citrus and its relatives in orchards and De Feyter, R., Y. Yang and D.W. Gabriel, 1993. Gene-for-genes forests of the endemic areas and application of biotechnology or interactions between cotton R genes and genetic engineering utilizing the knowledge on its molecular pv. malvacearum avr genes. Mol.Plant-Micr. Interact., 6: 225-237. mechanism of pathogenicity. Desai, V.T., S.A. Ranpise, C.V. Pujari and S.B. 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